Latent gene network expression underlies partial re-evolution of a polyphenic trait in the worker caste of ants

Polyphenisms—where alternative phenotypes develop from a single genome in response to environmental cues—are not only widespread in nature, but also occur at multiple levels of biological organization, from cells to individuals to societies. Polyphenism is thought to promote phenotypic diversification through the gain, loss, and re-evolution of alternative phenotypes. After the origin of a polyphenism, one of the alternative phenotypes often retains the developmental capacity to produce the ancestral trait, thereby permitting the other to evolve rapidly. Yet, little is known about the developmental processes underlying the re-evolution of polyphenic traits and how they may produce phenotypic diversification. Here we address this question by focusing on the caste polyphenism in ant societies, which produces a winged queen caste and a wingless worker caste in a single colony in response to environmental cues. We show, in a hyperdiverse group of ants, that a caste-specific trait called the ocelli (3 simple eyes on the dorsal head) is always present across queen castes but was lost and partially re-evolved multiple times, giving rise to novel patterns (1 ocelli) in the worker castes. Surprisingly, we discovered that a hidden (latent) expression of the ocelli gene regulatory network in worker castes that lost ocelli underlies the partial re-evolution of ocelli in this group. We therefore propose that latent developmental potentials may generally persist across polyphenic systems, including ant castes, and may facilitate the partial re-evolution of novel phenotypic patterns.